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Diet and breeding of the poorly known White-chinned Swift Cypseloides cryptus Zimmer, 1945, in Brazil

Diet and breeding of the poorly known White-chinned Swift Cypseloides cryptus Zimmer, 1945, in... Revista Brasileira de Ornitologia, 23(4), 398-404 ARTICLE December 2015 Diet and breeding of the poorly known White-chinned Swift Cypseloides cryptus Zimmer, 1945, in Brazil 1,6 1 1 1,2 5 Guilherme R. R. Brito , Daniel M. Figueira , Nelson Buainain , Daniel H. Firme , Renata N. Biancalana , 1 1 1 1 3 Claydson P. Assis , Gabriela G. Araujo , Marco A. Crozariol , Gabriella R. Frickes , Ricardo Parrini , 1,4 1 Piero A. Ruschi and Marcos A. Raposo Setor de Ornitologia, Departamento de Vertebrados, Museu Nacional, Universidade Federal do Rio de Janeiro. Quinta da Boa Vista s/n, São Cristóvão, CEP 20940-040, Rio de Janeiro, RJ, Brazil. Universidade de São Paulo, Instituto de Biociências, Departamento de Zoologia. Rua do Matão, Travessa 14, 101, Cidade Universitária, CEP 05508-090, São Paulo, SP, Brazil. Rua Hipólito da Costa, 53 ap. 101, Vila Isabel, Rio de Janeiro, RJ, Brazil. Setor de Ornitologia, Departamento de Zoologia, Museu de Biologia Prof. Mello Leitão/MBML, CEP 29650-000, Santa Teresa, ES, Brazil. Universidade Presbiteriana Mackenzie, Centro de Ciências Biológicas e da Saúde, Laboratório de Ecologia e Sistemática. Rua da Consolação, 930, Consolação, São Paulo, SP, Brazil. Corresponding author: grenzobrito@gmail.com Received on 13 March 2015. Accepted on 28 June 2015. ABSTRACT: The White-chinned Swift Cypseloides cryptus is perhaps one of the rarest swift species in the New World, and many aspects of its life history are poorly known. Here we report some new information on diet and reproductive behavior of a breeding population of C. cryptus at Asframa Falls, Rio Preto da Eva, Amazonas, Brazil. During four surveys at the breeding site (March and August 2012, July and August 2013), six active small cup-shaped nests were found and are described. Measurements and plumage information of five collected a dults and two chicks are also provided. Stomach contents (n=5) revealed the presence of insects of the order Hymenoptera and Hemiptera. The presence of a member of Psyllidae (Hemiptera) in the stomach contents suggests that this swift might also use a slightly different foraging strategy than commonly stated a bout swifts. Additionally, with this new information it is possible to determine the presence of the species over at least nine months in Brazil, indicating year-round residence. KEY-WORDS: Apodidae, Hemiptera, Hymenoptera, nest, stomach contents. Costa Rica, and Panama. In South America outside of INTRODUCTION Brazil, there are records from Peru, Ecuador, Colombia, Suriname, Venezuela (on the cordillera and tepuis) and The White-chinned Swift Cypseloides cryptus Zimmer, Guyana (Chantler 1999). 1945, might be one of the rarest swift species in the New World with fewer than 20 specimens collected from all parts of its known range (Kiff 1975). A dditionally, with METHODS only a few scarce observations in southern Central and northern South America (Chantler 1999), the natural history and distribution of the species are, unsurprisingly, The Asframa Falls (02°08'10.37"S, 59°59'46.46"W) still poorly known. (Figure 1A) is located in the Urubu river, municipality This bird occurs between sea level and 3000 m a.s.l. of Rio Preto da Eva, state of Amazonas, Brazil, c. 10 km Its main habitats are classified as montane and tropical distant from the Natal Waterfall breeding site discovered lowland evergreen forests, with a clear preference for gorges by Whittaker & Whittaker (2008). It is a recreational and waterfalls, which are used to nest and roost (Chantler area with a playground and two waterfalls, a large and a 1999). This swift was recently discovered in Brazil, in smaller one, surrounded by several acres of pristine forest. the municipality of Presidente Figueiredo, Amazonas The largest waterfall is approximately 5 m high and is State, where some individuals were observed breeding in formed by two levels, a short one c. 1 m high and a larger local waterfalls (Whittaker & Whittaker 2008). Central one with a fall of 4 m. American records are from Belize, Honduras, Nicaragua, The data presented here were gathered during four Revista Brasileira de Ornitologia, 23(4), 2015 Diet and breeding of the poorly known White-chinned Swift Cypseloides cryptus Zimmer, 1945, in Brazil Guilherme R. R. Brito et al. surveys at the breeding site (5 to 9 March and 9 to 15 dissected and stored in 70% ethanol. Each individual’s August 2012, 13 July and 17 August 2013). Collected stomach content was placed in a Petri dish and analyzed specimens (all fully-grown adults, being one male and with a stereomicroscope. Arthropods were identified four females) are housed in the ornithological collection to the lowest possible taxonomic level with help of of Museu Nacional/UFRJ, Rio de Janeiro, Brazil (MN). specialized literature (Rafael et al. 2012). Fragments Four specimens were prepared as study skins and one was were grouped and counted by morphological similarities, prepared as a “shmoo”, saving the full skeleton (Winker estimating the minimum number of prey of each taxa 2000) (Figure 1B). All carcasses were fixed in 4% formalin present in each sample. Digital photographs were taken and subsequently preserved in 70% ethanol; muscular using Canon Rebel XSi and Sony Cyber-Shot DSC-HX1 tissue samples were preserved in anhydrous ethanol. cameras, lens Sigma 150-500-mm, and cellular phone Two nests were dried and stored in the nest collection IPhone 4S. Nest measurements were taken using a digital (MNON-5482; MNON 5483); their classification caliper Mitutoyo Absolute and a measure tape. follows Simon & Pacheco (2005). Unfortunately, the small and delicate eggs were damaged during transport RESULTS AND DISCUSSION and could not be measured. The entire digestive tract was examined for food items, but remains were present in stomachs only. During the first field trip to Rio Preto da Eva, in March Stomachs were extracted from the abdominal cavity, 2012, a group of about 10 to 12 individuals of the White- A B C D FIGURE 1. A – Star = Asframa Falls, Rio Preto da Eva, Amazonas; B – White-chinned Swifts collected and housed in Museu Nacional/UFRJ, all fully-grown adults. MN 48599 – male with full skeleton preserved; MN 48597, 48598, 48600 and 48601 – females (Photo: Guilherme Brito); C – White-chinned Swift nest and egg collected and housed in Museu Nacional/UFRJ (Photo: Gabriella Frickes); D – Detail of possible undescribed plumage sexual dimorphism. Male on the left (MN 48599); female on the right (MN 48601); note white-tipped feathers on female’s abdomen (Photo: Guilherme Brito). Revista Brasileira de Ornitologia, 23(4), 2015 Diet and breeding of the poorly known White-chinned Swift Cypseloides cryptus Zimmer, 1945, in Brazil Guilherme R. R. Brito et al. chinned Swift was found using the rocky wall behind the pattern was found, and further work on collections with waterfall. On that occasion, five adult specimens, and specimens of the small and dark Cypseloides should be done two active nests, each containing one small and overall to confirm our suggestion. The suggestion that white tips white egg (Figure 1C), were collected by hand (see to the lower belly might be an indicative of immaturity measurements of birds and nests below). Other four nests (Schulenberg et al. 2007, Roesler et al. 2009) should also described in the present work (hereafter numbered N1 be investigated, because all specimens collected had fully – N4) were observed in the subsequent surveys in 2013, ossified skulls, indicating adulthood. but not collected, with features discussed below (Tables 1 and 2, Figure 2). Diet All specimens had good amount of accumulated fat on their interclavicle, abdominal, intercostal and In the stomach contents, we counted 36 prey items uropygium regions, with no visual difference between the among the five samples. The material was in an a dvanced individuals despite their differences in mass. stage of digestion and two of the five analyzed stomachs The measurements of the birds (Table 2) show that were completely empty (MN 48597; MN 48598 – the overall size of the male specimen is larger than those both females). The remaining three stomachs contained of the females and an interesting plumage pattern was 72.2% Hymenoptera (n = 26) and 27.8% Hemiptera (n observed on the abdominal area of the skins of adult = 10). We have also found some green moss (Bryophyta) specimens. All females have several feathers on that region fragments in two female samples (MN 48600; MN tipped white, while the only male has them uniformly 48601), but these were considered to have possibly been dark-brown and very few feathers tipped buff. This might ingested accidentally because the same material is used be an important and previously undescribed character of in nest construction. Most of the whole Hymenoptera sexual dimorphism in plumage (Figure 1D). Analyzing that allowed further identification were mainly winged specimens of adult Sooty Swifts Cypseloides fumigatus ants (Formicidae). All Hemiptera identified belonged to (Streubel, 1848) housed at the Museu Nacional, the same Psyllidae (jumping plant lice). TABLE 1. Measurements of five White-chinned Swift Cypseloides cryptus nests at Rio Preto da Eva, state of Amazonas, Brazil. N1 nest was only observed but not measured in time before being destroyed. 1 2 3 4 Nest Metrics NH (cm)H (cm)ND (cm)BW (cm) MNON 5482* 4.9 - 4.3 8 MNON 5483* 4.1 - 2.4 9.3 N2 4.6 255 2.7 14.5 N3 3.0 255 - 11.9 N4 3.4 255 - 8.5 1 2 3 NH = Nest height measured on the exterior from bottom to top; H = height from the ground to the nest; ND = internal nest depth; BW = nest width measured at the base. *Nests already dry, stored in the proper collection. MNON 5482 and MNON 5483 collected in March 2012. N2 – N4 nests observed in August 2013. TABLE 2. Measurements of the collected individuals of White-chinned Swift Cypseloides cryptus in Rio Preto da Eva, Amazonas State, Brasil. Catalog Number TL WS WL CH BL BH BW T Ta W Sex (mm) (mm) (mm) (mm) (mm) (mm) (mm) (mm) (mm) (g) MN48597 145 345 133.30 135 4.98 2.25 7 15.02 45 37 F MN48598 137 348 130.00 133 5.02 2.24 6.8 13.35 43 34 F MN48599 145 364 142.35 137 5.03 3 8 16.15 50 41 M MN48600 138 348 135.05 139 4.97 2.3 7.1 15 46 39 F MN48601 146 342 133.00 137 5.00 2.35 6.3 13.3 47 40 F TL = total length, WS = wing span, WL = wing length, CH = chord, BL = bill length (nostril to tip), BH = bill height (at the base), BW = bill width (at the base), T = tarsus, Ta = tail length, W = weight. Sex, mass, total length and wingspan taken in recently euthanized specimens. Remaining data after preparation (bill measures from the “schmoo” skin made on the carcass). Revista Brasileira de Ornitologia, 23(4), 2015 Diet and breeding of the poorly known White-chinned Swift Cypseloides cryptus Zimmer, 1945, in Brazil Guilherme R. R. Brito et al. FIGURE 2. Locations of White-chinned Swift’s studied nests (N1 – N4) on Asframa Falls, Rio Preto da Eva - Amazonas in 17 August 2013 (Photo: R. Biancalana). Such preference for preying upon winged individuals Swifts Chaetura brachyura (Jardine, 1846) were observed of Formicidae corroborates the report by Beebe (1949), slowing down their flight speed and taking unidentified who found “great quantities of Crematogaster and insects directly from the tree leaves near Manaus (R. P., Azteca flying ants” in the stomach of one specimen and pers. obs.). This could be a recurrent and rarely recorded “winged female Azteca ants” in another specimen of C. foraging strategy of swifts. Bull & Beckwith (1993) also cryptus. Howell (1957) observed c. 35 individuals of report Vaux’s Swifts Chaetura vauxi (Townsend, 1839) this species feeding in flight above the forest bor der at capturing insects from the tree canopy in the USA. a clearing in Nicaragua, where the stomach content of Although the hypothesis above is speculative to a one collected female was not identified, but believed certain degree, our data indicate its plausibility. The 30% to be Hymenoptera. Marín & Stiles (1992) reported of the diet by number composed by neither non-volant contents of four stomachs and two boluses with 91.7% nor swarming Psyllidae is noteworthy. In addition, these Hymenoptera (mainly Formicidae and Blastophagidae), insects are sessile and animals with these characteristics but the Psyllidae records reported here are new. are predated by closely related birds (Chaeturinae – Bull The presence of Psyllidae or “jumping plant louse” & Beckwith 1993). Further observations of this rare swift as one of the most important food items found in the and other Cypseloidinae might clarify this issue. stomachs gives us some interesting insights about foraging strategies of this species. As members of the Sternorrhyncha Breeding suborder, insects known to be relatively inactive for most of their lives (Borror et al. 1992), our findings suggest that Two nests were collected on 8 March 2012 attached to birds might use a different foraging strategy to reach and a rocky bed with one side leaning against the rocky wall consume them, rather than capturing swarming insects near the ceiling behind the waterfall, only accessible via during flight. Some swifts are known to catch aquatic a bypass where the water volume was reduced (Figure 2). insects in lakes and rivers by reducing their flight speed They consisted of a cup-shaped simple/platform (Simon sufficiently to permit them to grab individual prey items & Pacheco 2005) mainly constructed of moss, rootlets directly from the water surface (Chantler 1999). Similar and mud, which were humid due to constant water observations, not from water bodies, but on Amazonian sprinkle. Both nests contained a single sub-elliptical pure tree canopies were made when individuals of Short-tailed opaque white egg. On the occasion of the second survey, Revista Brasileira de Ornitologia, 23(4), 2015 Diet and breeding of the poorly known White-chinned Swift Cypseloides cryptus Zimmer, 1945, in Brazil Guilherme R. R. Brito et al. the water volume was greater compared to the first one A single nestling in its early stage of development due the advanced stage of the raining season, and despite was found in N3. It was not larger than 2 cm, had closed careful searches behind the waterfall, no individuals or eyes, overall dark sooty gray down and forehead feathers nests were found. in their sheaths. N4 was also active. The broo ding adult On 13 July 2013, RNB made a visit to the Asframa occupying this nest reacted to human approach by Falls and observed a flock of 5 to 6 in dividuals of White- conspicuously shaking its wings and ruffling its nape chinned Swifts foraging with Fork-tailed Palm-Swifts feathers. After a few minutes the adult left the nest Tachornis squamata (Cassin, 1853). One active nest (N1) enabling the observer to confirm t he presence of a chick, occupied by an adult individual (denoted by the dark which was in a more advanced stage of development than brown plumage with characteristic whitish facial marks) the chick in N3. Its body was covered with dark gray was found behind the upper part of the main fall. This downy plumage. The eyes were open and it had s luggish nest had a small cup shape and was of plant material, movements, occasionally moving the head towards the rootlets and leaves visibly damp on the exterior. flanks (Figure 3). No vocalization was hear d from the A subsequent visit to Asframa Falls made by RNB adults or nestlings during visits. on 17 Aug 2013 revealed the presence of two individuals Nests were in place and conditions similar to those foraging above the area of the falls as well as three described by Marín & Stiles (1992) and Whittaker & additional nests (N2 - N4) behind the fall, one of them Whittaker (2008). The main difference being the position empty, made of bryophytes, mud and fine rootlets. The and type of the nest described as a “low cup/lateral” for interior was lined with interwoven fine roots, sitting on a the latter, and in some aspects similar to those observed dry area of the lower part of the fall (N2). The nest seen in by Ayarzaguena (1984) and Marín & Stiles (1992) for July (N1) was found partially destroyed, and this was the the same species. The reuse of reproductive sites is well reason for the absence of measurement data for it (Figures known for species of Cypseloidinae (see Pichorim 2002). 2 and 3; Table 1). Regarding clutch size, Marín (1997) reports one-egg FIGURE 3. A. White-chinned Swift chick in N3 and, in the back, an adult in N4 (dashed circle). B. Chick with downy plumage in N4. Chicks with approximate age of ten to fifteen days (N3 younger than N4). Asframa Falls, Rio Preto da E va – Amazonas (Photos: R. Biancalana). Revista Brasileira de Ornitologia, 23(4), 2015 Diet and breeding of the poorly known White-chinned Swift Cypseloides cryptus Zimmer, 1945, in Brazil Guilherme R. R. Brito et al. clutch for both White-chinned and Spot-fronted Swifts, FAPERJ for GRRB’s PAPD/RJ postdoctoral fellowship Cypseloides cherriei Ridgway, 1893. (grant number E-26/102.506/2010); CNPq for PAR’s As expected for Cypseloidinae swifts, the nests were doctoral fellowship (grant number 140458/2012-3); and in dark and constantly humid areas, and the morphology, FAPESP for DHF’s doctoral fellowship (grant number composition and placement of the structures coincide 2012/00614-6); CNPq (grant number 307786/2011- with previous observations of this species and closely 0) and FAPERJ (grant number E-26/101.489/2010) for related ones (e.g. Spot-fronted Swift), where bryophytes, financial support to MAR. RNB is grateful to Vanilce mud and other vegetable fibers were used (Knorr 1961, Souza and Luiz Fernando Carvalho for support in the Foerster 1987, Marin & Stiles 1992, 1993). Also, these field and Fe lipe Bittioli R. Gomes for information on the elements have usually been assigned as differentiating nests. We are also very grateful to Jorge Nacinovic, Guy characters between Cypseloides and the remaining genera M. Kirwan and Bryan Jennings who kindly reviewed the within Apodidae, which do not use this particular kind English text, Michele Leocádio for help identifying food of vegetation associated with mud (Lack 1956, Whitacre items and Manuel Marín and GMK for useful comments 1989). on early versions of the manuscript. Based on Marín & Stiles (1992) description of White-chinned Swifts nestling development, we calculate that both chicks were around ten days to two weeks old, REFERENCES with the chick in N3 probably younger than the other. Ayarzaguena, J. 1984. Sobre la nidificación del vencejo castaño Therefore, considering the known nestling period for this (Cypseloides cryptus) (Aves: Apodidae). Memoria de la Sociedad de species (55–58 days, Marín & Stiles 1992), we estimate Ciencias Naturales La Salle, 122: 141−147. the fledging period of these chicks to be around late Beebe, W. 1949. The swifts of Rancho Grande, north-central September–mid October. Venezuela, with special reference to migration. Zoologica, 34: 53−62. The presence of one adult in the nest when chicks Biancalana, R. N. (2015). Breeding biology of the Sooty Swift are young, usually no more than three weeks old and Cypseloides fumigatus in São Paulo, Brazil. Wilson Journal of with the body mainly covered with downy feathers is a Ornitholog y, in press common characteristic of other Cypseloides species, such Borror, D. J.; Triplehorn, C. A. & Johnson, N. F. 1992. An th as the Sooty Swift (Biancalana 2015). introduction to the study of insects, 6 ed. Orlando: Harcourt Brace & Company. Our records from March to September and multiple Bull, E. L. & Beckwith, R. C. 1993. Diet and foraging behavior of observations in the region between Manaus and Presidente Vaux’s Swifts in northeastern Oregon. Condor, 95: 1016−1023. Figueiredo from July to November (Guy M. Kirwan, Chantler, P. 1999. Family Apodidae (swifts). pp. 388−457. In: del pers. comm.) testify the presence of White-chinned Swift Hoyo J.; Elliott, A. & Sargatal, J. (eds.) Handbook of birds of the world. Volume 5: Barn-owls to hummingbirds (eds.), Barcelona: for at least nine months (March–November) in Brazil, Lynx Edicions. with strong indications of successful breeding (used nests Foerster, K. S. 1987. The distribution and breeding biology of the Black from previous breeding seasons and fledging individual Swift (Cypseloides niger) in southern California. M.Sc. thesis. Long pictures in Whittaker & Whittaker 2008), and absence of Beach: California State University. seasonal migratory movements. Our results point to the Howell, T. R. 1957. Birds of a second-growth rain forest area of Nicaragua. Condor, 59(2): 73−111. importance of Hemiptera (Psyllidae) and Hymenoptera Kiff, L. F . 1975. Notes on southwestern Costa Rican birds. Condor, (Formicidae) insects in the diet, and confirm t he 77: 101−103. importance of waterfalls for nesting, which might prove Knorr, O. 1961. The geographical and ecological distribution of the helpful for further amplifying the knowledge about the Black Swift in Colorado. Wilson Bulletin, 73: 155−170. Lack, D. 1956. A review of the genera and nesting habits of swifts. distribution and natural history aspects of this elusive Auk, 73(1): 1−32. species. Marín, M. 1997. Some aspects of the breeding biology of the Black Swift. Wilson Bulletin, 109(2): 290−306. Marín, M. A. & Stiles, G. F. 1992. On the biology of five species of ACKNOWLEDGMENTS swifts (Apodidae, Cypseloidinae) in Costa Rica. Proceedings of the Western Foundation of Vertebrate Zoology, 4(5): 287−351. Marín, M. A. & Stiles, G. F. 1993. Notes on the biology of the Spot- To “Ecology and Environment do Brasil” for their help in fronted Swift. Condor, 95: 479−483. conducting, supporting and providing the logistics of the Pichorim, M. 2002. The breeding biology of the Biscutate surveys and ICMBio for the collecting permit (ICMBIO Swift (Streptoprocne biscutata) in southern Brazil. Ornitologia Neotropical, 13: 61−84. 10613). CAPES for granting MSc. Fellowships to Rafael, J. A.; Melo, G. A. R.; de Carvalho, C. J. B.; Casari, S. A. & DMF, GRF and GGA and doctoral fellowship to MAC; Constantino, R. 2012. Insetos do Brasil: diversidade e taxonomia. FAPERJ for CPA’s doctoral fellowship (grant number Ribeirão Preto: Holos Editora. E-26/101.489/2010) and NB’s scientific initiation Roesler, I.; Kirwan, G. M.; Agostini, M. A.; Beadle, D.; Shirihai, fellowship (grant number E-26/100.682/2012); CAPES/ H. & Binford, C. 2009. First sight records of White-chested Swift Cypseloides lemosi in Bolivia, with documented records of C. Revista Brasileira de Ornitologia, 23(4), 2015 Diet and breeding of the poorly known White-chinned Swift Cypseloides cryptus Zimmer, 1945, in Brazil Guilherme R. R. Brito et al. lemosi and White-chinned Swift C. cryptus in Peru. Bulletin of the Whittaker, A. & Whittaker, S. A. 2008. The White-chinned Swift British Ornithologists’ Club, 129(4): 222−228. Cypseloides cryptus (Apodiformes: Apodidae) breeding near Schulenberg, T. S.; Stotz, D. F.; Lane, D. F.; O’Neill, J. P. & Parker, Presidente Figueiredo, Amazonas: the first documented record for T. A. 2007. Birds of Peru. Princeton: Princeton University Press. Brazil. Revista Brasileira de Ornitologia, 16(4): 398−401. Simon, J. E. & Pacheco, F. 2005. On the standardization of nest Winker, K. 2000. Obtaining, preserving, and preparing bird descriptions of Neotropical birds. Revista Brasileira de Ornitologia, specimens. Journal of Field Ornithology, 71(2): 250−297. 13(2): 143−154. Whitacre, D. F. 1989. Conditional use of nest structures by White- naped and White-collared Swifts. Condor, 91: 813−125. Associate Editor: Leandro Bugoni Revista Brasileira de Ornitologia, 23(4), 2015 http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png Ornithology Research Springer Journals

Diet and breeding of the poorly known White-chinned Swift Cypseloides cryptus Zimmer, 1945, in Brazil

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Revista Brasileira de Ornitologia, 23(4), 398-404 ARTICLE December 2015 Diet and breeding of the poorly known White-chinned Swift Cypseloides cryptus Zimmer, 1945, in Brazil 1,6 1 1 1,2 5 Guilherme R. R. Brito , Daniel M. Figueira , Nelson Buainain , Daniel H. Firme , Renata N. Biancalana , 1 1 1 1 3 Claydson P. Assis , Gabriela G. Araujo , Marco A. Crozariol , Gabriella R. Frickes , Ricardo Parrini , 1,4 1 Piero A. Ruschi and Marcos A. Raposo Setor de Ornitologia, Departamento de Vertebrados, Museu Nacional, Universidade Federal do Rio de Janeiro. Quinta da Boa Vista s/n, São Cristóvão, CEP 20940-040, Rio de Janeiro, RJ, Brazil. Universidade de São Paulo, Instituto de Biociências, Departamento de Zoologia. Rua do Matão, Travessa 14, 101, Cidade Universitária, CEP 05508-090, São Paulo, SP, Brazil. Rua Hipólito da Costa, 53 ap. 101, Vila Isabel, Rio de Janeiro, RJ, Brazil. Setor de Ornitologia, Departamento de Zoologia, Museu de Biologia Prof. Mello Leitão/MBML, CEP 29650-000, Santa Teresa, ES, Brazil. Universidade Presbiteriana Mackenzie, Centro de Ciências Biológicas e da Saúde, Laboratório de Ecologia e Sistemática. Rua da Consolação, 930, Consolação, São Paulo, SP, Brazil. Corresponding author: grenzobrito@gmail.com Received on 13 March 2015. Accepted on 28 June 2015. ABSTRACT: The White-chinned Swift Cypseloides cryptus is perhaps one of the rarest swift species in the New World, and many aspects of its life history are poorly known. Here we report some new information on diet and reproductive behavior of a breeding population of C. cryptus at Asframa Falls, Rio Preto da Eva, Amazonas, Brazil. During four surveys at the breeding site (March and August 2012, July and August 2013), six active small cup-shaped nests were found and are described. Measurements and plumage information of five collected a dults and two chicks are also provided. Stomach contents (n=5) revealed the presence of insects of the order Hymenoptera and Hemiptera. The presence of a member of Psyllidae (Hemiptera) in the stomach contents suggests that this swift might also use a slightly different foraging strategy than commonly stated a bout swifts. Additionally, with this new information it is possible to determine the presence of the species over at least nine months in Brazil, indicating year-round residence. KEY-WORDS: Apodidae, Hemiptera, Hymenoptera, nest, stomach contents. Costa Rica, and Panama. In South America outside of INTRODUCTION Brazil, there are records from Peru, Ecuador, Colombia, Suriname, Venezuela (on the cordillera and tepuis) and The White-chinned Swift Cypseloides cryptus Zimmer, Guyana (Chantler 1999). 1945, might be one of the rarest swift species in the New World with fewer than 20 specimens collected from all parts of its known range (Kiff 1975). A dditionally, with METHODS only a few scarce observations in southern Central and northern South America (Chantler 1999), the natural history and distribution of the species are, unsurprisingly, The Asframa Falls (02°08'10.37"S, 59°59'46.46"W) still poorly known. (Figure 1A) is located in the Urubu river, municipality This bird occurs between sea level and 3000 m a.s.l. of Rio Preto da Eva, state of Amazonas, Brazil, c. 10 km Its main habitats are classified as montane and tropical distant from the Natal Waterfall breeding site discovered lowland evergreen forests, with a clear preference for gorges by Whittaker & Whittaker (2008). It is a recreational and waterfalls, which are used to nest and roost (Chantler area with a playground and two waterfalls, a large and a 1999). This swift was recently discovered in Brazil, in smaller one, surrounded by several acres of pristine forest. the municipality of Presidente Figueiredo, Amazonas The largest waterfall is approximately 5 m high and is State, where some individuals were observed breeding in formed by two levels, a short one c. 1 m high and a larger local waterfalls (Whittaker & Whittaker 2008). Central one with a fall of 4 m. American records are from Belize, Honduras, Nicaragua, The data presented here were gathered during four Revista Brasileira de Ornitologia, 23(4), 2015 Diet and breeding of the poorly known White-chinned Swift Cypseloides cryptus Zimmer, 1945, in Brazil Guilherme R. R. Brito et al. surveys at the breeding site (5 to 9 March and 9 to 15 dissected and stored in 70% ethanol. Each individual’s August 2012, 13 July and 17 August 2013). Collected stomach content was placed in a Petri dish and analyzed specimens (all fully-grown adults, being one male and with a stereomicroscope. Arthropods were identified four females) are housed in the ornithological collection to the lowest possible taxonomic level with help of of Museu Nacional/UFRJ, Rio de Janeiro, Brazil (MN). specialized literature (Rafael et al. 2012). Fragments Four specimens were prepared as study skins and one was were grouped and counted by morphological similarities, prepared as a “shmoo”, saving the full skeleton (Winker estimating the minimum number of prey of each taxa 2000) (Figure 1B). All carcasses were fixed in 4% formalin present in each sample. Digital photographs were taken and subsequently preserved in 70% ethanol; muscular using Canon Rebel XSi and Sony Cyber-Shot DSC-HX1 tissue samples were preserved in anhydrous ethanol. cameras, lens Sigma 150-500-mm, and cellular phone Two nests were dried and stored in the nest collection IPhone 4S. Nest measurements were taken using a digital (MNON-5482; MNON 5483); their classification caliper Mitutoyo Absolute and a measure tape. follows Simon & Pacheco (2005). Unfortunately, the small and delicate eggs were damaged during transport RESULTS AND DISCUSSION and could not be measured. The entire digestive tract was examined for food items, but remains were present in stomachs only. During the first field trip to Rio Preto da Eva, in March Stomachs were extracted from the abdominal cavity, 2012, a group of about 10 to 12 individuals of the White- A B C D FIGURE 1. A – Star = Asframa Falls, Rio Preto da Eva, Amazonas; B – White-chinned Swifts collected and housed in Museu Nacional/UFRJ, all fully-grown adults. MN 48599 – male with full skeleton preserved; MN 48597, 48598, 48600 and 48601 – females (Photo: Guilherme Brito); C – White-chinned Swift nest and egg collected and housed in Museu Nacional/UFRJ (Photo: Gabriella Frickes); D – Detail of possible undescribed plumage sexual dimorphism. Male on the left (MN 48599); female on the right (MN 48601); note white-tipped feathers on female’s abdomen (Photo: Guilherme Brito). Revista Brasileira de Ornitologia, 23(4), 2015 Diet and breeding of the poorly known White-chinned Swift Cypseloides cryptus Zimmer, 1945, in Brazil Guilherme R. R. Brito et al. chinned Swift was found using the rocky wall behind the pattern was found, and further work on collections with waterfall. On that occasion, five adult specimens, and specimens of the small and dark Cypseloides should be done two active nests, each containing one small and overall to confirm our suggestion. The suggestion that white tips white egg (Figure 1C), were collected by hand (see to the lower belly might be an indicative of immaturity measurements of birds and nests below). Other four nests (Schulenberg et al. 2007, Roesler et al. 2009) should also described in the present work (hereafter numbered N1 be investigated, because all specimens collected had fully – N4) were observed in the subsequent surveys in 2013, ossified skulls, indicating adulthood. but not collected, with features discussed below (Tables 1 and 2, Figure 2). Diet All specimens had good amount of accumulated fat on their interclavicle, abdominal, intercostal and In the stomach contents, we counted 36 prey items uropygium regions, with no visual difference between the among the five samples. The material was in an a dvanced individuals despite their differences in mass. stage of digestion and two of the five analyzed stomachs The measurements of the birds (Table 2) show that were completely empty (MN 48597; MN 48598 – the overall size of the male specimen is larger than those both females). The remaining three stomachs contained of the females and an interesting plumage pattern was 72.2% Hymenoptera (n = 26) and 27.8% Hemiptera (n observed on the abdominal area of the skins of adult = 10). We have also found some green moss (Bryophyta) specimens. All females have several feathers on that region fragments in two female samples (MN 48600; MN tipped white, while the only male has them uniformly 48601), but these were considered to have possibly been dark-brown and very few feathers tipped buff. This might ingested accidentally because the same material is used be an important and previously undescribed character of in nest construction. Most of the whole Hymenoptera sexual dimorphism in plumage (Figure 1D). Analyzing that allowed further identification were mainly winged specimens of adult Sooty Swifts Cypseloides fumigatus ants (Formicidae). All Hemiptera identified belonged to (Streubel, 1848) housed at the Museu Nacional, the same Psyllidae (jumping plant lice). TABLE 1. Measurements of five White-chinned Swift Cypseloides cryptus nests at Rio Preto da Eva, state of Amazonas, Brazil. N1 nest was only observed but not measured in time before being destroyed. 1 2 3 4 Nest Metrics NH (cm)H (cm)ND (cm)BW (cm) MNON 5482* 4.9 - 4.3 8 MNON 5483* 4.1 - 2.4 9.3 N2 4.6 255 2.7 14.5 N3 3.0 255 - 11.9 N4 3.4 255 - 8.5 1 2 3 NH = Nest height measured on the exterior from bottom to top; H = height from the ground to the nest; ND = internal nest depth; BW = nest width measured at the base. *Nests already dry, stored in the proper collection. MNON 5482 and MNON 5483 collected in March 2012. N2 – N4 nests observed in August 2013. TABLE 2. Measurements of the collected individuals of White-chinned Swift Cypseloides cryptus in Rio Preto da Eva, Amazonas State, Brasil. Catalog Number TL WS WL CH BL BH BW T Ta W Sex (mm) (mm) (mm) (mm) (mm) (mm) (mm) (mm) (mm) (g) MN48597 145 345 133.30 135 4.98 2.25 7 15.02 45 37 F MN48598 137 348 130.00 133 5.02 2.24 6.8 13.35 43 34 F MN48599 145 364 142.35 137 5.03 3 8 16.15 50 41 M MN48600 138 348 135.05 139 4.97 2.3 7.1 15 46 39 F MN48601 146 342 133.00 137 5.00 2.35 6.3 13.3 47 40 F TL = total length, WS = wing span, WL = wing length, CH = chord, BL = bill length (nostril to tip), BH = bill height (at the base), BW = bill width (at the base), T = tarsus, Ta = tail length, W = weight. Sex, mass, total length and wingspan taken in recently euthanized specimens. Remaining data after preparation (bill measures from the “schmoo” skin made on the carcass). Revista Brasileira de Ornitologia, 23(4), 2015 Diet and breeding of the poorly known White-chinned Swift Cypseloides cryptus Zimmer, 1945, in Brazil Guilherme R. R. Brito et al. FIGURE 2. Locations of White-chinned Swift’s studied nests (N1 – N4) on Asframa Falls, Rio Preto da Eva - Amazonas in 17 August 2013 (Photo: R. Biancalana). Such preference for preying upon winged individuals Swifts Chaetura brachyura (Jardine, 1846) were observed of Formicidae corroborates the report by Beebe (1949), slowing down their flight speed and taking unidentified who found “great quantities of Crematogaster and insects directly from the tree leaves near Manaus (R. P., Azteca flying ants” in the stomach of one specimen and pers. obs.). This could be a recurrent and rarely recorded “winged female Azteca ants” in another specimen of C. foraging strategy of swifts. Bull & Beckwith (1993) also cryptus. Howell (1957) observed c. 35 individuals of report Vaux’s Swifts Chaetura vauxi (Townsend, 1839) this species feeding in flight above the forest bor der at capturing insects from the tree canopy in the USA. a clearing in Nicaragua, where the stomach content of Although the hypothesis above is speculative to a one collected female was not identified, but believed certain degree, our data indicate its plausibility. The 30% to be Hymenoptera. Marín & Stiles (1992) reported of the diet by number composed by neither non-volant contents of four stomachs and two boluses with 91.7% nor swarming Psyllidae is noteworthy. In addition, these Hymenoptera (mainly Formicidae and Blastophagidae), insects are sessile and animals with these characteristics but the Psyllidae records reported here are new. are predated by closely related birds (Chaeturinae – Bull The presence of Psyllidae or “jumping plant louse” & Beckwith 1993). Further observations of this rare swift as one of the most important food items found in the and other Cypseloidinae might clarify this issue. stomachs gives us some interesting insights about foraging strategies of this species. As members of the Sternorrhyncha Breeding suborder, insects known to be relatively inactive for most of their lives (Borror et al. 1992), our findings suggest that Two nests were collected on 8 March 2012 attached to birds might use a different foraging strategy to reach and a rocky bed with one side leaning against the rocky wall consume them, rather than capturing swarming insects near the ceiling behind the waterfall, only accessible via during flight. Some swifts are known to catch aquatic a bypass where the water volume was reduced (Figure 2). insects in lakes and rivers by reducing their flight speed They consisted of a cup-shaped simple/platform (Simon sufficiently to permit them to grab individual prey items & Pacheco 2005) mainly constructed of moss, rootlets directly from the water surface (Chantler 1999). Similar and mud, which were humid due to constant water observations, not from water bodies, but on Amazonian sprinkle. Both nests contained a single sub-elliptical pure tree canopies were made when individuals of Short-tailed opaque white egg. On the occasion of the second survey, Revista Brasileira de Ornitologia, 23(4), 2015 Diet and breeding of the poorly known White-chinned Swift Cypseloides cryptus Zimmer, 1945, in Brazil Guilherme R. R. Brito et al. the water volume was greater compared to the first one A single nestling in its early stage of development due the advanced stage of the raining season, and despite was found in N3. It was not larger than 2 cm, had closed careful searches behind the waterfall, no individuals or eyes, overall dark sooty gray down and forehead feathers nests were found. in their sheaths. N4 was also active. The broo ding adult On 13 July 2013, RNB made a visit to the Asframa occupying this nest reacted to human approach by Falls and observed a flock of 5 to 6 in dividuals of White- conspicuously shaking its wings and ruffling its nape chinned Swifts foraging with Fork-tailed Palm-Swifts feathers. After a few minutes the adult left the nest Tachornis squamata (Cassin, 1853). One active nest (N1) enabling the observer to confirm t he presence of a chick, occupied by an adult individual (denoted by the dark which was in a more advanced stage of development than brown plumage with characteristic whitish facial marks) the chick in N3. Its body was covered with dark gray was found behind the upper part of the main fall. This downy plumage. The eyes were open and it had s luggish nest had a small cup shape and was of plant material, movements, occasionally moving the head towards the rootlets and leaves visibly damp on the exterior. flanks (Figure 3). No vocalization was hear d from the A subsequent visit to Asframa Falls made by RNB adults or nestlings during visits. on 17 Aug 2013 revealed the presence of two individuals Nests were in place and conditions similar to those foraging above the area of the falls as well as three described by Marín & Stiles (1992) and Whittaker & additional nests (N2 - N4) behind the fall, one of them Whittaker (2008). The main difference being the position empty, made of bryophytes, mud and fine rootlets. The and type of the nest described as a “low cup/lateral” for interior was lined with interwoven fine roots, sitting on a the latter, and in some aspects similar to those observed dry area of the lower part of the fall (N2). The nest seen in by Ayarzaguena (1984) and Marín & Stiles (1992) for July (N1) was found partially destroyed, and this was the the same species. The reuse of reproductive sites is well reason for the absence of measurement data for it (Figures known for species of Cypseloidinae (see Pichorim 2002). 2 and 3; Table 1). Regarding clutch size, Marín (1997) reports one-egg FIGURE 3. A. White-chinned Swift chick in N3 and, in the back, an adult in N4 (dashed circle). B. Chick with downy plumage in N4. Chicks with approximate age of ten to fifteen days (N3 younger than N4). Asframa Falls, Rio Preto da E va – Amazonas (Photos: R. Biancalana). Revista Brasileira de Ornitologia, 23(4), 2015 Diet and breeding of the poorly known White-chinned Swift Cypseloides cryptus Zimmer, 1945, in Brazil Guilherme R. R. Brito et al. clutch for both White-chinned and Spot-fronted Swifts, FAPERJ for GRRB’s PAPD/RJ postdoctoral fellowship Cypseloides cherriei Ridgway, 1893. (grant number E-26/102.506/2010); CNPq for PAR’s As expected for Cypseloidinae swifts, the nests were doctoral fellowship (grant number 140458/2012-3); and in dark and constantly humid areas, and the morphology, FAPESP for DHF’s doctoral fellowship (grant number composition and placement of the structures coincide 2012/00614-6); CNPq (grant number 307786/2011- with previous observations of this species and closely 0) and FAPERJ (grant number E-26/101.489/2010) for related ones (e.g. Spot-fronted Swift), where bryophytes, financial support to MAR. RNB is grateful to Vanilce mud and other vegetable fibers were used (Knorr 1961, Souza and Luiz Fernando Carvalho for support in the Foerster 1987, Marin & Stiles 1992, 1993). Also, these field and Fe lipe Bittioli R. Gomes for information on the elements have usually been assigned as differentiating nests. We are also very grateful to Jorge Nacinovic, Guy characters between Cypseloides and the remaining genera M. Kirwan and Bryan Jennings who kindly reviewed the within Apodidae, which do not use this particular kind English text, Michele Leocádio for help identifying food of vegetation associated with mud (Lack 1956, Whitacre items and Manuel Marín and GMK for useful comments 1989). on early versions of the manuscript. Based on Marín & Stiles (1992) description of White-chinned Swifts nestling development, we calculate that both chicks were around ten days to two weeks old, REFERENCES with the chick in N3 probably younger than the other. Ayarzaguena, J. 1984. 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On the biology of five species of ACKNOWLEDGMENTS swifts (Apodidae, Cypseloidinae) in Costa Rica. Proceedings of the Western Foundation of Vertebrate Zoology, 4(5): 287−351. Marín, M. A. & Stiles, G. F. 1993. Notes on the biology of the Spot- To “Ecology and Environment do Brasil” for their help in fronted Swift. Condor, 95: 479−483. conducting, supporting and providing the logistics of the Pichorim, M. 2002. The breeding biology of the Biscutate surveys and ICMBio for the collecting permit (ICMBIO Swift (Streptoprocne biscutata) in southern Brazil. Ornitologia Neotropical, 13: 61−84. 10613). CAPES for granting MSc. Fellowships to Rafael, J. A.; Melo, G. A. R.; de Carvalho, C. J. B.; Casari, S. A. & DMF, GRF and GGA and doctoral fellowship to MAC; Constantino, R. 2012. Insetos do Brasil: diversidade e taxonomia. FAPERJ for CPA’s doctoral fellowship (grant number Ribeirão Preto: Holos Editora. E-26/101.489/2010) and NB’s scientific initiation Roesler, I.; Kirwan, G. M.; Agostini, M. A.; Beadle, D.; Shirihai, fellowship (grant number E-26/100.682/2012); CAPES/ H. & Binford, C. 2009. First sight records of White-chested Swift Cypseloides lemosi in Bolivia, with documented records of C. Revista Brasileira de Ornitologia, 23(4), 2015 Diet and breeding of the poorly known White-chinned Swift Cypseloides cryptus Zimmer, 1945, in Brazil Guilherme R. R. Brito et al. lemosi and White-chinned Swift C. cryptus in Peru. Bulletin of the Whittaker, A. & Whittaker, S. A. 2008. The White-chinned Swift British Ornithologists’ Club, 129(4): 222−228. Cypseloides cryptus (Apodiformes: Apodidae) breeding near Schulenberg, T. S.; Stotz, D. F.; Lane, D. F.; O’Neill, J. P. & Parker, Presidente Figueiredo, Amazonas: the first documented record for T. A. 2007. Birds of Peru. Princeton: Princeton University Press. Brazil. Revista Brasileira de Ornitologia, 16(4): 398−401. Simon, J. E. & Pacheco, F. 2005. On the standardization of nest Winker, K. 2000. Obtaining, preserving, and preparing bird descriptions of Neotropical birds. Revista Brasileira de Ornitologia, specimens. Journal of Field Ornithology, 71(2): 250−297. 13(2): 143−154. Whitacre, D. F. 1989. Conditional use of nest structures by White- naped and White-collared Swifts. Condor, 91: 813−125. Associate Editor: Leandro Bugoni Revista Brasileira de Ornitologia, 23(4), 2015

Journal

Ornithology Research – Springer Journals

Published: Dec 1, 2015

Keywords: Apodidae; Hemiptera; Hymenoptera; nest; stomach contents

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